A comparison of the immunological response in zebrafish and rainbow trout infected with fish parasite, Ichthyophthirius multifiliis

Ichthyophthirius multifiliis, the causative agent of white spot disease, is associated with high mortality, morbidity, and significant economic losses in both the aquaculture and ornamental fish industries. I. multifiliis exhibits low host specificity, infecting nearly all freshwater fish species, with severe cases reported in rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and channel catfish (Ictalurus punctatus). In contrast, zebrafish (Danio rerio) display a high level of natural resistance to the parasite. The immunological mechanisms underlying this resistance are not fully understood, though it has been suggested that early immune responses during infection may influence disease severity. Understanding these early responses and the mechanisms of natural resistance could aid in mitigating the disease and provide insights into protective immunity. The aim of this study was to investigate the early immunological response to I. multifiliis infection in naturally resistant zebrafish and susceptible rainbow trout using transcriptomics. Zebrafish and rainbow trout were infected with I. multifiliis, and gill samples were collected at 2, 24, 48, and 72 hours post-infection (hpi) for transcriptomic analysis. Results showed that zebrafish mounted a strong immune response, peaking at 24 hpi with 1,231 differentially expressed (DE) genes, before returning to normal levels. In contrast, rainbow trout exhibited a much weaker response, with only 28 DE genes at 24 hpi, and the response normalized by 72 hpi. In zebrafish, DE genes were associated with six immune-related pathways, however all DE genes were significantly downregulated, suggesting that the zebrafish may have cleared the infection early, negating the need for further immune activation. This was confirmed by a decrease in the number of transcripts mapping to the I. multifiliis genome in zebrafish, however, in rainbow trout the number of mapping transcripts increased over time indicating disease progression. Several cytokines related to cellular immune responses, such as Cxcl8a, Cxcl13, and Cxcl11, were upregulated, highlighting the role of immune cells in combating I. multifiliis. Overall, this study supports the idea that early immune responses are critical in determining the severity of I. multifiliis infection.